This article was downloaded by: [Mauro Cosolo]On: 06 October 2011, At: 23:27Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House,37-41 Mortimer Street, London W1T 3JH, UK

Bird StudyPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/tbis20

Dietary changes of Mediterranean Shags Phalacrocoraxaristotelis desmarestii between the breeding and post-breeding seasons in the upper Adriatic SeaMauro Cosolo a , Nicoletta Privileggi a , Barbara Cimador a & Stefano Sponza aa Department of Life Sciences, University of Trieste, via Giorgieri 9, I–34127, Trieste, Italy

Available online: 04 Aug 2011

To cite this article: Mauro Cosolo, Nicoletta Privileggi, Barbara Cimador & Stefano Sponza (2011): Dietary changes ofMediterranean Shags Phalacrocorax aristotelis desmarestii between the breeding and post-breeding seasons in the upperAdriatic Sea, Bird Study, DOI:10.1080/00063657.2011.603290

To link to this article: http://dx.doi.org/10.1080/00063657.2011.603290

PLEASE SCROLL DOWN FOR ARTICLE

Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form toanyone is expressly forbidden.

The publisher does not give any warranty express or implied or make any representation that the contentswill be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses shouldbe independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims,proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly inconnection with or arising out of the use of this material.

Dietary changes of Mediterranean ShagsPhalacrocorax aristotelis desmarestii between thebreeding and post-breeding seasons in the upperAdriatic Sea

MAURO COSOLO, NICOLETTA PRIVILEGGI, BARBARA CIMADOR and STEFANO SPONZA∗

Department of Life Sciences, University of Trieste, via Giorgieri 9, I–34127, Trieste, Italy

Capsule Shags move between breeding and non-breeding areas and this is associated with a significantchange in diet.Aims To determine whether the diet of Shags nesting on islets off the Croatian coast is the same as theirdiet after the post-breeding move to the Gulf of Trieste.Methods Diet was determined by the analysis of 611 regurgitated food pellets.Results A total of 23 988 prey items were identified in the sample of pellets. Post-breeding Shags in theGulf of Trieste focused on demersal and relatively immobile Gobiidae (81.5% by number, 87.1% by bio-mass). The most frequent prey species was Gobius niger (70.8% by number). In the breeding season atOruda island, Croatia, the diet was more varied. Breeding Shags fed on bentho-pelagic, mobile preysuch as Atherina boyeri (28.4% in frequency), Serranus hepatus (16.1%) and Crenilabrus tinca(12.0%), while Gobiidae had a dietary frequency of only 18.1%. With respect to biomass the most impor-tant prey were Crenilabrus tinca (19.0%) and Serranus hepatus (18.4%).Conclusion We suggest that the movement of Shags within the Adriatic Sea is driven by dietary require-ments. Most previous studies of Shag diet have shown that Shags tend to have a more specialized dietduring the breeding season, concentrating upon demersal prey species. However, we have found thatbirds breeding at the Croatian study colony show dietary diversity. We suggest that lack of dietary special-ization is a facultative response to local prey abundance, and is probably the result of over-fishing of demer-sal species in the areas around the breeding locations in which the birds find suitable sites and are littledisturbed by human activity. Shags may move immediately after breeding to the Gulf of Trieste becausedemersal species are likely to be more abundant there. As a consequence, the diet becomes more special-ized and is then more similar to the diet of other populations of Shags.

Seabirds are key players at the top of marine food chains

and respond predictably to alterations in prey abundance.

They have therefore been used as reliable indicators of

changes in fish populations (Hatch & Sanger 1992, Mon-

tevecchi 1993, Furness & Camphuysen 1997, Barrett

2002). Changes in a variety of seabird foraging parameters

have been successfully used to detect alterations in prey

age–class structure (Davoren & Montevecchi 2003),

responses of prey populations to climate change (Miller

& Sydeman 2004), and variations in the energetic

value of prey (Wanless et al. 2005). Furthermore, seabirds’

dietary adjustments may indicate shifts in pelagic food

webs (Montevecchi & Myers 1996).

European Shags Phalacrocorax aristotelis are foot-pro-

pelled diving seabirds (Ashmole 1971), whose diet has

been used to assess the recruitment and abundance of

fish populations (Barrett et al. 1990, Barrett 1991). In

Iceland the diet of this species was used as a measure-

ment of the recruitment in commercially important

fish species such as Saithe Pollachius virens and Plaice

Pleuronectes platessa (Lilliendahl & Solmundsson

2006). Shag diet varies depending on annual changes

in prey availability (Carss 1993) and, to a lesser

extent, on location. The species feeds on a wide range

of benthic, demersal and schooling pelagic fish, and for∗Correspondence author. Email: sponza@units.it

Q 2011 British Trust for Ornithology

Bird Study (2011) iFirst, 1–12

Dow

nloa

ded

by [

Mau

ro C

osol

o] a

t 23:

27 0

6 O

ctob

er 2

011

this reason it is classified as opportunistic in its feeding

habits (Barrett 1991, Gremillet et al. 1998, Velando &

Freire 1999). Foraging areas have depths ranging

between 7 and 80 m (Guyot 1988, Barrett & Furness

1990, Wanless et al. 1991a, 1993a), with a mean of

30 m (Wanless et al. 1997a), and are usually between

7 and 17 km around the breeding colonies (Wanless

et al. 1991b). The average daily food consumption of a

Shag is between 16 and 24% of body mass (Barrett

et al. 1990). During incubation, Shags are estimated to

have an average daily requirement of 389 g of fish,

while a bird with three chicks requires about 920 g

(Wanless et al. 1993b). The diet of the species has

been studied as early as the first half of the last century

(Steven 1933), mainly in north-western Europe. In

this area the Atlantic subspecies P. aristotelis aristotelisis distributed from Iceland and Northern Scandinavia

to the Iberian Peninsula (Nelson 2005). The analysis

of dispersal patterns suggests that Iberian Shags are iso-

lated from northern populations (Velando 1997,

Velando & Freire 1999). Sandeels Ammodytes spp. dom-

inate the diet of P. aristotelis aristotelis, both in summer

(Barrett et al. 1986, Gremillet et al. 1998, Furness &

Tasker 2000) and in other seasons (Harris & Wanless

1991). Exceptions to Sandeel dominance were found

in Norway, where Gadoids (Gadidae) were the most

important prey (Barrett et al. 1990). In Iceland Shags

rely heavily on Lesser Sandeels Ammodytes marinusduring the breeding season, whereas Bull-rout Myoxoce-phalus scorpius and Gadoids become increasingly impor-

tant in autumn and winter (Lilliendahl &

Solmundsson 2006). Sandeels are also the dominant

prey on the Galician coast of north-west Spain

(Velando & Freire 1999). In this area some seasonal

differences in diet have been found; in February and

March Shags foraged on Gobiidae and Sand Smelts

Atherina presbyter and this dietary change may be due

to the seasonal changes in the abundance of Sandeel

schools. In northern Spain breeding Shags fed on Labri-

dae and Atherinidae (Alvarez 1998).

Even though the Atlantic subspecies is well studied,

very little is known of the diet, general biology and popu-

lation of the Mediterranean subspecies P. aristotelis des-marestii, which is endemic to the Mediterranean and

Black Seas. The breeding range includes most States

along the Mediterranean coast (Croatia, Albania, Bul-

garia, Ukraine, Turkey, Cyprus, Egypt, Libya, Tunisia

and Algeria). The total population has been estimated

at less than 10 000 pairs, half of them breeding within

the eastern coast of Spain, Baleares, Corsica, Sardinia,

the Tuscany archipelago, Lampedusa, Crete and the

islets of the Ionian Sea. Substantial year-to-year fluctu-

ations in breeding numbers have been reported in

several colonies, and there appears to be an overall

decrease (Aguilar & Fernandez 2002). This occurs

mainly because Mediterranean Shags are severely

affected by a number of limiting factors, including

human disturbance (Guyot 1993), chemical pollution

(Lambertini & Leonzio 1986), oil spills (Velando et al.2005) and accidental catch (Aguilar 1991, Velando &

Freire 2002). The subspecies is consequently listed in

Annex I of the Birds Directive 147/2009 and is the

focus of an Action Plan (Aguilar & Fernandez 2002).

To our knowledge, the available data for the diet of

the species in the whole Mediterranean rely on the

study of Guyot (1988) on the Corsican population,

which suggested that Labridae and Ammodytidae were

the most important prey. However, a small sample of

chick regurgitations from some Sardinian breeding colo-

nies showed the presence of a wider range of species in

the diet, including Crenilabrus sp., Mullus surmuletus,Coris julis, Mugil sp., Serranus sp., Sardina pilchardus and

Boops salpa (Brichetti et al. 1992).

In the Adriatic Sea, Mediterranean Shags breed in

Croatia (2000 pairs) and Albania (5–10 pairs)

(Aguilar & Fernandez 2002). From the 1980s onward,

the species has become a regular summer visitor in the

Gulf of Trieste, north east Italy, with increasing

numbers (Utmar 1999). The maximum size of the popu-

lation approached 2500 individuals in July 2007. This

population comes mainly from the Croatian breeding

colonies (Sponza et al. 2010). Because of the high sensi-

tivity of Shags to human disturbance during breeding

(Guyot 1993), the Gulf of Trieste does not offer suitable

and low disturbed places for nesting, but these character-

istics are to be found within the Croatian islets. Given

Mediterranean Shags’ conservation status and the very

few studies on this subspecies, we have determined the

diet during the breeding season in Croatia and the

post-breeding period in the Gulf of Trieste. We use

this dietary information to suggest reasons why Shags

breed in Croatia but spend the post-breeding period in

another area of the Adriatic Sea.

METHODS

Study area

We studied the diet of Mediterranean Shags during the

breeding season (January–April) at Oruda island

(Losinj archipelago) (44833′N, 14830′E), one of the

most important Croatian colonies in the upper Adriatic

Q 2011 British Trust for Ornithology, Bird Study, iFirst, 1–12

2 M. Cosolo et al.

Dow

nloa

ded

by [

Mau

ro C

osol

o] a

t 23:

27 0

6 O

ctob

er 2

011

Sea. In this rocky, low-vegetated island, covering an area

of 36 ha, about 100 breeding pairs nest inside bushes of

Paliurus spina-Christi and Crataegus monogyna near the

sea. The diet of the species in the post-breeding period

(May–October) was studied in the Gulf of Trieste

(45839′N, 13846′E). The two study areas have very

different sea bottom depth profiles. The Gulf of Trieste

is 20 m deep within 1 km of the coastline and deepest

at 25 m. The Losinj archipelago is characterized by a

steep, sloping sea bed. The eastern part of the archipe-

lago is 40–45 m deep within a few metres of the coast-

line and reaches a maximum depth of 80 m.

Conversely, the western side is characterized by shal-

lower depths (20–25 m).

Diet analysis

Diet was characterized by pellet analysis, a non-invasive

method that can provide large samples over time.

Dietary data were described in a preliminary way by

Sponza et al. (2010), in which the key prey were ident-

ified by pellet analysis and linked with diving strategies,

and this in turn served to characterize the different fora-

ging habitats and benefits of dives. In this paper the

entire data set is used for a comprehensive analysis of

the diet of Mediterranean Shags during the breeding

and post-breeding seasons.

Pellet collection involves little or no disturbance to

birds and analyses require minimal laboratory facilities

(Carss et al. 1997). This method has been widely used

to characterize the diet composition of Cormorants,

Shags, Gulls, Terns and Skuas (reviewed in Barrett

et al. 2007) and to estimate body sizes and biomasses of

the prey eaten (Duffy & Jackson 1986, Dirksen et al.1995, Velando & Freire 1999, Eschbaum et al. 2003,

Gagliardi et al. 2007, Barquete et al. 2008). However,

the analysis of pellets has to consider the partial erosion

of otoliths caused by the digestive process, so fish

lengths derived from otoliths could be under-estimates

(Johnstone et al. 1990, Carss et al. 1997). Moreover, the

smallest otoliths (i.e. belonging to very small fish) could

be completely digested (Johnstone et al. 1990) and

otolith wear can vary from bird to bird or from time to

time, so the validity of the technique will vary with the

species. For example, it was shown that Gadidae, unlike

Ammodytidae, have very robust otoliths (Barrett et al.1990). However, the potential degree of otolith erosion

for most of the North Adriatic fish species has not yet

been characterized. Unlike some invasive method

(Duffy & Jackson 1986, Carss et al. 1997), pellet analysis

has been recognized as an appropriate method for the

temporal and spatial comparison of the diet of Shags

(Duffy & Laurenson 1983, Barrett et al. 1990, Barrett

1991), and it is to this purpose that we use data based

upon these techniques in this article.

In the Gulf of Trieste, during the 2005 post-breeding

period (May–October), we collected 23–30 pellets per

month at each of the three roosts, except for May at

the beginning of the season (14–15 pellets) (Table 1).

The three roosts are: Isonzo river mouth (45843′N,

13833′E), Filtri (45844′N, 13839′E) and Lazzaretto

(45836′N, 13842′E). At the first site Shags roost on

beached, dead trees and sand banks, while in the latter

two sites, birds rest on floating platforms used for

mussel farming. We used a canoe to reach sand banks,

beached trunks, and floating platforms, minimizing dis-

turbance to birds. We analysed a total of 486 items. In

Croatia, during the 2006 breeding season (January–

April) we analysed a total of 125 pellets (Table 2), col-

lected monthly near the nests at the Oruda colony.

During the monthly visits we observed adult birds in

breeding plumage only. All samples were fresh and

showed no signs of deterioration. Upon collection, all

specimens were individually sealed in a plastic bag and

tagged with an identification number and then stored

and frozen until processing. The probability of analysing

pellets regurgitated by the same individual was negli-

gible, given the high numbers of Shags present in the

two study areas, and given that each collection was

carried out in different sites and periods.

We processed all pellets in the laboratory following a

dissolution method described by Privileggi (2003). Each

pellet was individually stored in a beaker (50 ml), soaked

in a detergent solution, and then left to settle for about

20 hours. After the mucous had been dissolved, Isopod

parasites and Nematode worms were removed and,

after decanting, otoliths and any skeletal structures

useful for prey identification were separated out. We

used a filter in order not to lose the smallest otoliths

during the outflow. To remove any mucous residue

and to bleach bones, each sample was treated with a sol-

ution of sodium hydroxide (NaOH, 10%) and sodium

hypochlorite (NaClO, 50%). This method ensured the

conservation of the smallest bony fragments during the

mucous dissolution. We then rinsed all samples with

water and air dried them at room temperature before

storage and examination. Where possible, we paired oto-

liths. We also accurately separated and identified

(according to our own reference collection and to Har-

konen 1986, Keller 1993, Veldkamp 1995) otoliths,

scales, opercula and vertebrae to the lowest taxonomic

Q 2011 British Trust for Ornithology, Bird Study, iFirst, 1–12

Diet of Mediterranean Shags 3

Dow

nloa

ded

by [

Mau

ro C

osol

o] a

t 23:

27 0

6 O

ctob

er 2

011

Table 1. Dietary composition of Mediterranean Shags Phalacrocorax aristotelis desmarestii in the Gulf of Trieste during the 2005 post-breeding season, expressed as numerical frequency (%N), biomass (%B) andfrequency of occurrence (%O) percentage values.

May June July August September October

No. of pellets44 89 90 90 90 83

No. of prey1207 2613 3503 4591 4110 4692

%N %B %O %N %B %O %N %B %O %N %B %O %N %B %O %N %B %O

GobiidaeGobius niger 56.42 39.97 100.00 71.76 44.10 100.00 80.02 51.66 100.00 62.88 54.93 100.00 77.20 48.77 100.00 69.29 60.70 96.40Zosterisessor ophiocephalus 5.80 29.07 65.90 6.77 33.29 89.70 6.54 28.12 85.50 6.69 28.34 90.00 11.92 32.96 92.20 4.26 19.88 83.10Gobius bucchichii 9.78 3.79 54.50 7.65 3.31 52.30 1.88 1.18 30.00 0.35 0.26 13.30 0.75 0.48 20.00 0.40 0.35 13.20Gobius cruentatus 2.90 8.80 45.40 1.80 5.22 31.80 0.94 3.24 23.30 0.63 3.92 22.20 0.39 2.03 14.40 0.15 1.30 6.00Gobius cobitis 0.25 1.35 6.80 0.50 2.92 11.30 0.31 2.14 11.10 0.09 1.68 3.30 0.32 3.77 13.30 0.13 2.40 6.00Pomatoschistus minutus – – – 0.04 0.02 1.10 0.03 0.01 1.10 – – – 0.02 0.00 11.10 0.40 0.16 10.80Pomatoschistus marmoratus – – – 0.38 0.09 6.80 0.03 0.01 1.10 0.48 0.18 7.80 0.29 0.05 10.00 0.06 0.02 3.60TriglidaeLepidotrigla cavillone – – – – – – – – – 0.02 0.01 1.10 – – – – – –CepolidaeCepola rubescens 1.08 3.16 25.00 1.15 2.78 25.00 1.34 3.33 22.20 0.74 2.73 18.90 0.95 4.23 22.20 0.94 5.06 24.10PleuronectidaePlatichthys flesus 0.17 0.57 2.30 – – – 0.03 0.19 1.10 0.35 1.06 3.30 – – – – – –SoleidaeSolea vulgaris – – – – – – 0.31 0.35 5.50 0.15 0.09 2.20 0.44 0.38 6.60 1.13 0.99 7.20SparidaeOblada melanura 0.08 0.18 2.30 – – – 0.03 0.13 1.10 – – – – – – – – –Diplodus sargus – – – – – – 0.03 0.12 1.10 – – – – – – – – –Diplodus annularis – – – – – – 0.03 0.27 1.10 – – – – – – 0.04 0.24 2.40Pagellus erythrinus 1.24 1.02 6.80 – – – 0.06 0.07 2.20 – – – – – – 0.64 0.91 10.80Pagrus pagrus 0.08 0.48 2.30 – – – – – – – – – – – – – – –Dentex dentex – – – – – – – – – 0.02 0.15 1.10 – – – – – –Lithognathus mormyrus – – – – – – – – – 0.09 0.34 1.10 – – – – – –Boops salpa 0.17 0.31 2.30 – – – 0.03 0.09 1.10 – – – – – – – – –LabridaeCrenilabrus tinca 1.08 0.60 15.90 1.91 1.06 19.30 0.77 0.73 24.40 0.78 0.52 25.50 0.41 0.19 10.00 0.60 0.61 16.80SerranidaeSerranus hepatus 8.12 6.64 45.40 2.64 2.65 37.50 2.37 3.06 37.80 0.96 1.34 18.90 1.56 2.38 31.10 0.40 0.73 12.00GadidaeTrysopterus minutus 1.82 0.31 11.30 1.19 0.16 15.90 0.66 1.21 17.80 0.37 0.94 16.70 1.07 2.82 20.00 0.23 0.81 9.60Odontogadus merlangus 0.33 0.03 4.50 0.46 0.62 4.50 0.06 0.05 1.10 – – – 0.05 0.90 1.10 0.02 0.03 1.20Maenidae 0.58 0.65 9.10 0.46 0.62 10.20 0.09 0.22 2.20 0.13 0.42 3.30 0.10 0.18 1.10 0.13 0.38 2.40EngraulidaeEngraulis encrasicholus 1.24 0.62 13.60 2.22 2.23 19.30 1.26 2.29 18.90 0.41 0.93 8.90 0.44 0.48 12.20 0.21 0.24 2.40Mugilidae – – – – – – – – – – – – – – – 0.09 0.93 1.20AtherinidaeAtherina boyeri 8.37 1.72 18.20 0.80 0.22 7.90 2.74 0.82 5.50 24.40 1.71 37.80 3.99 0.17 10.00 20.74 3.90 53.00CarangidaeTrachurus mediterraneus 0.41 0.70 9.10 0.19 0.36 4.50 0.34 0.26 6.60 0.46 0.44 3.30 0.10 0.20 3.30 0.13 0.37 2.40MoronidaeDicentrarchus labrax 0.08 0.04 2.30 – – – – – – – – – – – – – – –SphyraenidaeSphyraena sphyraena – – – 0.04 0.06 1.10 0.09 0.40 2.20 – – – – – – – – –BelonidaeBelone belone – – – 0.04 0.30 1.10 0.03 0.07 1.10 – – – – – – – – –

Q2011

BritishTrustfor

Ornitholog

y,Bird

Study,

iFirst,1

–12

4M

.C

osoloetal.

Dow

nloa

ded

by [

Mau

ro C

osol

o] a

t 23:

27 0

6 O

ctob

er 2

011

Table 2. Dietary composition of Mediterranean Shags Phalacrocorax aristotelis desmarestii at the breeding colony at Oruda, Croatia, during the 2006 breeding season, expressed asnumerical frequency (%N), biomass (%B) and frequency of occurrence (%O) percentage values.

January February March April

No. of pellets30 30 30 35

No. of prey900 758 971 643

%N %B %O %N %B %O %N %B %O %N %B %O

GobiidaeGobius niger 10.67 2.83 66.60 5.01 1.24 44.80 30.07 4.30 76.60 13.84 2.40 58.80Zosterisessor ophiocephalus 0.11 1.16 3.30 – – – – – – – – –Gobius bucchichii – – – – – – 0.10 0.07 3.30 – – –Gobius cruentatus – – – 0.13 0.66 3.40 – – – – – –Pomatoschistus minutus 1.89 0.15 10.00 0.26 0.01 3.40 2.27 0.15 6.60 – – –Pomatoschistus marmoratus 0.67 0.09 6.60 0.79 0.04 13.80 2.16 0.08 16.60 – – –CepolidaeCepola rubescens 0.33 3.09 3.30 2.11 5.35 6.90 9.78 25.64 26.60 4.04 3.94 2.90SoleidaeSolea vulgaris 0.22 0.38 3.30 – – – – – – – – –ScorpaenidaeScorpaena scrofa – – – – – – 0.10 0.59 3.30 – – –BothidaeArnoglossus laterna – – – – – – 0.21 0.29 6.60 – – –SparidaeSparus auratus – – – – – – – – – 0.31 2.22 5.80Oblada melanura – – – 2.11 10.96 13.80 0.21 0.91 6.60 1.40 6.38 5.80Diplodus sargus 0.11 3.82 3.30 0.92 1.26 3.40 – – – – – –Diplodus annularis 1.89 7.89 20.00 5.54 16.23 44.80 0.93 3.05 13.30 0.93 3.93 14.70Charax puntazzo 0.11 1.22 3.30 – – – – – – – – –Pagellus erythrinus 8.00 13.68 56.60 5.28 6.72 37.90 7.62 11.53 50.00 16.02 17.09 64.70Lithognathus mormyrus 0.11 2.42 3.30 0.13 0.97 3.40 – – – 1.24 9.63 11.70LabridaeCrenilabrus tinca 9.11 16.67 60.00 3.83 11.58 62.10 12.67 18.29 83.30 24.73 27.23 94.10SerranidaeSerranus hepatus 13.33 17.15 46.60 23.75 31.22 65.50 18.64 21.09 63.30 7.15 6.56 38.20Maenidae 6.89 19.02 36.60 5.80 5.94 37.90 5.05 9.98 40.00 5.29 11.55 41.10EngraulidaeEngraulis encrasicholus – – – – – – 0.41 0.76 3.30 0.31 0.46 5.80Mugilidae – – – 1.06 1.57 3.40 – – – – – –AtherinidaeAtherina boyeri 45.11 8.89 60.00 40.90 4.10 48.30 8.34 1.12 46.60 20.68 2.39 38.20CarangidaeTrachurus mediterraneus – – – – – – – – – 0.16 0.40 2.90MoronidaeDicentrarchus labrax 1.44 1.56 36.60 2.37 2.15 34.50 1.44 2.16 33.30 3.58 2.21 23.50ScombridaeScomber scomber – – – – – – – – – 0.31 3.60 5.80

Q20

11

BritishTrustfor

Ornitholog

y,Bird

Study,iFirst,

1–12

DietofM

editerraneanShag

s5

Dow

nloa

ded

by [

Mau

ro C

osol

o] a

t 23:

27 0

6 O

ctob

er 2

011

level, by using a stereomicroscope with an ocular

micrometer (6–32× zoom lens). The reference collec-

tion of diagnostic bones (Privileggi 2003) includes 79

marine (1107 individuals) and 45 freshwater fish

species (1465 individuals) of different size classes. We

evaluated the total length and mass of each prey by

means of both original (Privileggi 2003) and published

(Keller 1993, Volponi 1994, Veldkamp 1995) equations

that relate otoliths length to the body size and the mass

of fish. We produced an equation for each fish species,

except Cepola rubescens, Belone belone, Gobius bucchichiiand Sphyraena sphyraena, which were excluded from

this analysis. While analysing eroded otoliths, particular

attention was paid to the comparison of the morphologi-

cal characters of outline, sulcus, rostrum and ostium with

the reference collection, in order to estimate and adjust

the size of the otoliths.

The level of taxonomic resolution for identification

was different for some prey types. In this paper we

treated the family Mugilidae as one category, as the

species that make up this family are difficult to identify

because of the extreme similarity of the otoliths. More-

over, the family Maenidae is represented essentially by

Maena maena and Maena chryselis, whereas many families

are represented by one species only (i.e. Atherinidae by

Atherina boyeri, Labridae by Crenilabrus tinca, Serranidae

by Serranus hepatus) (Tables 1 & 2).

Each prey type in the diet was estimated as numerical

frequency (N), biomass (B), and frequency of occurrence

(O, number of samples containing each prey type). Con-

tingency tables tested by chi-square test (x2) were used

to compare the numerical frequencies (not percentages)

of different prey types between the two study areas and

the monthly differences within each area. For this

purpose, we grouped the different prey species by

family. Families representing less than 1% at both

study areas were categorized as ‘Other species’. Other

statistical differences were assessed with Mann–

Whitney U test and Spearman’s rank correlation.

As regards prey size, we report the descriptive analysis

only. Consequently we do not compare the two study

areas and the different months within each study area,

in order not to go beyond the limits of the pellet analysis

method.

The significance threshold was set at P , 0.05 and

the analysis was performed using SPSS 13.0 and STATIS-

TICA 7.1 software.

RESULTS

Analysis of 611 pellets revealed 23 988 identified prey.

Of these, 20 716 belonged to 31 taxa in the Gulf of

Trieste, whereas 3272 belonged to 26 taxa in Croatia

(Tables 1 & 2). In the Gulf of Trieste, Gobiidae were

the focal prey (81.5%N). The most captured species

was the Black Goby Gobius niger (70.8%N), which

occurred (%O) in 99.2% of the pellets analysed. The

second in importance (11.9%N) were Atherinidae (i.e.

Atherina boyeri) (Table 1). Conversely, in Croatia,

Atherinidae were the most important prey (28.4%N),

followed by Gobiidae (18.1%N), Serranidae (16.1%N)

(i.e. Serranus hepatus), Labridae (12.0%N)

(i.e. Crenilabrus tinca), and Sparidae (12.6%N) (Fig. 1,

Table 2).

Diet composition was significantly different between

the two study areas (x2 ¼ 8894.5, df ¼ 8, P , 0.0001)

(Fig. 1). The main contributions to the total Chi-square

were given by 5 (Sparidae, Gobiidae, Serranidae, Labri-

dae, Maenidae) over nine categories. However, the

main contributions were first due to the high consump-

tion of Sparidae (family contribution/total contri-

bution ¼ 1860.7/8894.5) and then to the low

consumption of Gobiidae (family contribution/total

contribution 1346.3/8894.5) in Croatia with respect to

Table 3. Descriptive analysis of prey size (fish length, cm) in the diet of Mediterranean Shags Phalacrocorax aristotelis desmarestii in the Gulf ofTrieste and at the breeding colony at Oruda, Croatia.

Family

Gulf of Trieste Croatia

N Mean sd Min. Max. Mode N Mean sd Min. Max. Mode

Atherinidae 2475 5.02 1.82 2.25 10.91 4 930 5.55 1.62 2.96 11.08 4Gobiidae 16 430 7.87 2.95 1.47 24.60 6 591 4.36 1.62 1.58 18.74 4Labridae 171 7.59 1.96 3.18 14.57 7 393 9.49 2.42 6.36 23.94 8Maenidae 42 11.16 3.31 5.76 27.52 9, 10 197 9.49 3.73 1.83 21.25 8Moronidae 1 – – – – – 68 10.28 1.94 6.46 15.65 10Serranidae 377 8.78 1.13 5.36 11.57 8 527 8.31 0.66 6.27 10.55 8Sparidae 62 10.94 4.12 5.88 22.07 9 411 12.10 4.51 3.95 25.10 9All families 20 051 7.61 3.03 1.47 29.03 6 3131 7.54 3.58 1.58 25.10 4, 8

Q 2011 British Trust for Ornithology, Bird Study, iFirst, 1–12

6 M. Cosolo et al.

Dow

nloa

ded

by [

Mau

ro C

osol

o] a

t 23:

27 0

6 O

ctob

er 2

011

the Gulf of Trieste. In this latter area, the differences

between months were significant (x2 ¼ 2463.9, df ¼

40, P , 0.0001). In the context of a huge exploitation

of Gobiidae, both by number and biomass (Table 1, Fig.

1), the monthly differences in frequency were principally

due to Atherinidae during the whole period (family con-

tribution/total contribution ¼ 1649.8/2463.9). Such

differences were particularly evident in August, when

we recorded at the same time the lowest frequencies

(with respect to the expected values) for Gobiidae

(monthly family contribution/monthly total contri-

bution ¼ 60.5/692.9) and the highest for Atherinidae

(monthly family contribution/monthly total contri-

bution ¼ 595.5/692.9). A high consumption of Serrani-

dae was recorded in May (monthly family contribution/monthly total contribution ¼ 263.2/385.9).

In Croatia, the differences between months were sig-

nificant (x2 ¼ 879.8, df ¼ 24, P , 0.0001). Atherini-

dae (family contribution/total contribution ¼ 280.9/

879.8), Gobiidae (family contribution/total contri-

bution ¼ 223.2/879.8), and Labridae (family contri-

bution/total contribution ¼ 135.5/879.8) contributed

the most to the differences. The highest contribution

was due to March, when we observed an increase in

the consumption of Gobiidae (monthly family contri-

bution/monthly total contribution ¼ 146.3/371.1)

and a concurrent decrease of Atherinidae (monthly

family contribution/monthly total contribution ¼

137.8/371.1).

In order to assess a possible relationship between fre-

quency and biomass values, we correlated the overall

data for the two study areas (Fig. 2). We found a signifi-

cant correlation in the Gulf of Trieste only (Spearman’s

rank correlation: NGulf of Trieste ¼ 9, rs ¼ 0.88, P , 0.01;

NCroatia ¼ 9, rs ¼ 0.35, P ¼ 0.36). However, at both

sites, we showed two atypical points of the two more

abundant taxa (circles in Fig. 2a), that are Gobiidae

and Atherinidae. In Croatia, the effect of both values

Figure 1. Numerical frequency (%N) and biomass (%B) percentages of prey in the diet of Mediterranean Shags Phalacrocorax aristotelis des-marestii in the Gulf of Trieste and at Oruda breeding colony, Croatia. Fish families are listed in the key.

Q 2011 British Trust for Ornithology, Bird Study, iFirst, 1–12

Diet of Mediterranean Shags 7

Dow

nloa

ded

by [

Mau

ro C

osol

o] a

t 23:

27 0

6 O

ctob

er 2

011

lead to high frequency and low biomass values. In the

Gulf of Trieste this trend was confirmed by Atherinidae,

while a high frequency of Gobiidae corresponded to high

biomass values. If we removed these exceptions, the two

regressions became similar and overlapping (Spearman’s

rank correlation: NGulf of Trieste ¼ 7, rs ¼ 0.96, P ,

0.001; NCroatia ¼ 9, rs ¼ 0.86, P , 0.02) (Fig. 2b).

Considering the ecology of prey (benthic, bentho-

pelagic and pelagic), we found significant differences

between the two areas (x2 ¼ 7213.2, df ¼ 2, P ,

0.0001). In the Gulf of Trieste, Shags strongly preferred

benthic fishes, both in terms of frequency (83.0%) and

biomass (91.2%), whereas in Croatia there was a

higher consumption of bentho-pelagic prey (frequency

46.4%, biomass 78.0%). In fact the main contributions

to the total Chi-square were due to the low frequency

of benthic (category contribution/total contribution ¼

1194.1/7213.2) and a high consumption of bentho-

pelagic prey (category contribution/total contribution

¼ 4526.6/7213.2) in Croatia.

We determined a prey size mode of 6 cm in the Gulf of

Trieste, whereas in Croatia we recorded two modal sizes,

at 4 and 8 cm. The larger prey sizes are recorded in May

and June. Moreover, prey lengths decreased significantly

within the season (Spearman’s rank correlation: n ¼ 6,

rs ¼ – 0.83, P , 0.05) (Fig. 3).

DISCUSSION

European Shags are opportunistic predators, and the

variability in composition of their diet in different

locations is related to geographical differences in the

available potential prey (Barrett 1991, Velando &

Freire 1999). Moreover, the species has a high flexibility

Figure 2. (a) Frequency/biomass correlations in the two study areas. Black points indicate values for each one of the nine fish families. Blackcircles indicate the value for Gobiidae, while dashed circles indicate Atherinidae. (b) Frequency/biomass correlations with Gobiidae and Ather-inidae values removed (Cep, Cepolidae; Lab, Labridae; Mae, Maenidae; Mor, Moronidae; Oth, Other species; Ser, Serranidae; Spa, Sparidae).

Q 2011 British Trust for Ornithology, Bird Study, iFirst, 1–12

8 M. Cosolo et al.

Dow

nloa

ded

by [

Mau

ro C

osol

o] a

t 23:

27 0

6 O

ctob

er 2

011

of feeding grounds, both in terms of diving depths and

bottom sediment characteristics (Guyot 1988, Wanless

et al. 1991b, Velando & Freire 1999). Our study

supports this evidence. Recognizing the limitations of

the pellet analyses used, we highlight a wide prey spec-

trum, mostly composed of fish species that are found at

a diversity of depths and in different habitats, including

pelagic prey (such as Atherina boyeri), bentho-pelagic

fishes from sandy and rocky bottoms (such as Pagelluserythrinus and Serranus hepatus) and demersal species

from sandy-mud bottoms (such as the family Gobiidae).

We never observed Shags following fishing trawlers

nor feeding on by-catch discards. As also reported by

Oro & Ruiz (1997) and Arcos et al. (2002), we consider

this behaviour as very occasional in our study

population.

Are Shags really opportunistic predators?

Although Shags have flexible feeding habits that

allow them to exploit both benthic and pelagic

resources (Gremillet et al. 1998), they should be con-

sidered as predominantly benthic feeders (Cramp &

Simmons 1977, Barrett et al. 1990, Wanless et al.1991a, 1993a, 1998, Watanuki et al. 2008). Diet ana-

lyses in most of Europe actually show that Shags rely

on Sandeels (Ammodytes spp.) (Barrett et al. 1986,

Harris & Wanless 1991, 1993, Gremillet et al. 1998,

Velando & Freire 1999, Furness & Tasker 2000, Lil-

liendahl & Solmundsson 2006). Even if Sandeels some-

times form schools within the water column (Jonsson

1992), Shags catch these prey on or near the bottom

(Harris & Wanless 1991, Wanless et al. 1991a,

1997b). We confirm the importance of the sea bed

for Mediterranean Shags, by showing that these birds

exploit prey in the Gulf of Trieste which are essentially

benthic. Similarly, in Croatia, Shags forage mostly

(69.0% by number) on benthic and bentho-pelagic

fishes. Moreover, we emphasize that, from May to

October, the period with the larger presence of Shags

(Sponza et al. 2010), the Gulf of Trieste is one of the

most important Adriatic areas for the abundance of

pelagic ephemeral species such as Engraulis encrasicolus,Sardina pilchardus and Scomber scomber. In late spring,

these species leave the central Adriatic areas and

reach the Gulf of Trieste’s shallow waters for spawning

(Skrivanic & Zavodnik 1973, Orel & Zamboni 2004).

While they represent 74% of the north Adriatic fish

landings (Prestamburgo et al. 2005), these fishes rep-

resent less than 1% and 0.5% by number of Shags’

diet in the Gulf of Trieste and Croatia, respectively.

We therefore suggest that Shags aim at diving towards

the sea bed to exploit mainly benthic, but also

bentho-pelagic, food resources, and do not take advan-

tage of abundant pelagic prey.

Diet specialization

Sandeels play a key role in the diet of Shags in most

European waters and are the basis of a feeding specializ-

ation during the chick rearing period (Harris & Wanless

1993, Velando & Freire 1999). This specialization is

probably linked to the high energetic value and the

abundance of these fishes, which also represent the

focal prey of many seabird species (Rindorf et al.2000). Contrary to what has been found in most

studies, we did not find any prey specialization during

the breeding season. Rather, in Croatia, the prey spec-

trum is particularly wide, as we recorded the prevailing

importance of five families (Sparidae, Gobiidae, Serrani-

dae, Labridae, Maenidae).

The role of Gobiidae

Feeding specialization is conversely recorded during the

post-breeding period. In the Gulf of Trieste, Shags

indeed focused on demersal Gobiidae, both in terms of

frequency (81.5%) and biomass (87.1%). We report

slight exceptions to such dominance in August and

October, when there was a decrease of Gobiidae and

an increase in Atherinidae. The species belonging to

both families are sedentary and perform short move-

ments (Riedl 1991). Gobiidae are strictly demersal and

Figure 3. Monthly mean (+ sd) size (length of fish, cm) of prey con-sumed by Mediterranean Shags Phalacrocorax aristotelis desmarestiiin the Gulf of Trieste and at Oruda breeding colony, Croatia.

Q 2011 British Trust for Ornithology, Bird Study, iFirst, 1–12

Diet of Mediterranean Shags 9

Dow

nloa

ded

by [

Mau

ro C

osol

o] a

t 23:

27 0

6 O

ctob

er 2

011

poor swimmers (Louisy 2005), whereas Atherinidae are

confined in estuaries and coastal lagoons (Louisy

2005). They aggregate in schools which lay at different

depths (Riedl 1991). Given the role of Gobiidae, the

possible temporary differences in the availability of

these demersal prey could lead Shags to forage in the

upper layers of the water column as well, thus exploiting

other fish. Similarly, Lilliendahl & Solmundsson (2006)

noted momentary changes in Shags’ diet as a conse-

quence of possible variations in the availability of their

focal prey (Sandeels). Shags also shift between Gobiidae

and Atherinidae in Croatia during March. The signifi-

cant increase of Gobiidae could be linked to the

Shags’ efforts to focus on these demersal prey. Since

the April data do not substantiate a further increment,

this pattern could be simply linked to a temporary acces-

sibility of these fishes. The likely non-prevalence of a

fish species over another could lead Croatian Shags to

exploit the currently available prey, which would bring

about an increase in dietary diversity. This is particularly

evident in March and April, which is at the peak of

chick rearing (Sponza et al. 2010). It is important to

stress that Lilliendahl & Solmundsson (2006) recorded

a high dietary overlap between nestlings and adult

Shags in Iceland. Moreover, Velando & Freire (1999),

even if suggesting some differences in diet between nest-

lings and adults in Spain, showed that chicks were fed

almost exclusively with Sandeels. In May and June,

the main chick rearing period in Spain, Sandeels rep-

resented more than 80% by number of adults’ diet. We

hence maintain that Shags’ dietary variability in

Croatia reflected nestlings’ diet.

The importance of Gobiidae can also be inferred from

the analysis of frequency/biomass ratio, which highlights

how these prey are a discriminating factor at both study

areas. If we remove Gobiidae values, the diet indeed

tends to a similar frequency/biomass ratio in the two

areas. On the contrary, we record a positive effect of

Gobiidae in the Gulf of Trieste only. This is due to

the larger size of Gobies in the Gulf of Trieste with

respect to Croatia.

Prey size

Prey sizes are slightly shorter by comparison with the

prey of Shags breeding in Scotland (9.7 cm) (Wanless

et al. 1993a) and Spain (9.8 cm) (Velando & Freire

1999). The most frequent prey length in the Gulf of

Trieste is 6 cm, whereas in Croatia we detected two

modes (4 and 8 cm length), which are similar to the

modal lengths (6 and 8 cm) recorded by Wanless et al.(1993b).

Nonetheless, the most interesting aspect is the trend of

the monthly mean size of prey between the two areas. We

suggest that there is an increase in prey length at the end

of the breeding season (April) which is probably linked to

chick rearing. Conversely, larger prey are taken in May

and June in the Gulf of Trieste. Thereafter, the prey size

decreases. We could assume that this trend is probably

related to an abundance of adult Gobies in May and

June due to spawning (Patzner 2007).

Ecological perspectives

Shags summering in the Gulf of Trieste come from the

Croatian breeding colonies (Sponza et al. 2010). These

post-breeding movements are linked to a more profitable

foraging activity in the Gulf of Trieste with respect to

Croatian waters, due to shallower depths (maximum

25 m versus 80 m in Croatia) and reduced physiological

stress during diving (Sponza et al. 2010). These move-

ments have not been always a habitual pattern, since

they increased consistently from the 1980s to become

a real migratory movement at the present time (Sponza

et al. 2010). During the 1980s and 1990s, there was a

substantial decrease (67%) of demersal fisheries landings

along the eastern Adriatic Sea coastline (Slovenia,

Croatia, Bosnia-Herzegovina, Montenegro and

Albania) (Mannini et al. 2005). We suggest that there

has been over-fishing in Croatian waters and the inten-

sive use of unselective bottom trawls have lead to a

shortage of demersal fish, thus reducing the probability

of Shags showing feeding specialization during breeding.

The consequent necessity to exploit bentho-pelagic

resources possibly forced Shags to a broader and more

variable diet. Conversely, although feeding specializ-

ation is attainable in the Gulf of Trieste, Shags cannot

nest there because of human disturbance and a lack of

suitable sites. Nonetheless, the specialization on demer-

sal Gobiidae allows Shags to efficiently recover from the

costs of the breeding season in Croatia (Sponza et al.2010).

This study suggests that the diet of Mediterranean

Shags can be used to index the availability of fish in

marine ecosystems (Thayer & Sydeman 2007, Mills

et al. 2007) and to provide useful information about

the fish resource conditions that can be incorporated

in fisheries management models (Hislop & Harris

1985, Hatch & Sanger 1992, Barrett 2002, Roth et al.2007).

Q 2011 British Trust for Ornithology, Bird Study, iFirst, 1–12

10 M. Cosolo et al.

Dow

nloa

ded

by [

Mau

ro C

osol

o] a

t 23:

27 0

6 O

ctob

er 2

011

ACKNOWLEDGEMENTS

We thank C. Trani for help in collecting pellets. Particular

thanks are due to J. Kralj and M. Kulieri’c of the Institute of

Ornithology of Zagreb (Croatia) for permissions and logistic

support. At Veli Losinj (Croatia) we thank Blue World staff,

in particular N. Rako, P. Makelworth and Karlo, for bringing

us to and from Oruda island. A PhD scholarship was granted to

B. Cimador by the University of Trieste. We finally thank

E.A. Ferrero for valuable criticism and we are also indebted

to the anonymous reviewers for constructive suggestions and

comments on a previous version.

REFERENCES

Aguilar, J.S. 1991. Resum de l’Atlas d’ocells marins de les Balears,1991. Anuari Ornitologic de les Baleares 6: 17–28.

Aguilar, J.S. & Fernandez, G. 2002. Species Action Plan for the Med-iterranean Shag (Phalacrocorax aristotelis desmarestii). Conventionon the Conservation of European Wildlife and Natural Habitats, Stras-bourg, December 2002. BirdLife International, Cambridge, UK.

Alvarez, D. 1998. The diet of shags (Phalacrocorax aristotelis L.) in theCantabrian Sea (North of Spain) during the breeding season. Seabird20: 22–30.

Arcos, J.M., Ruiz, X., Bearhop, S. & Furness, R.W. 2002. Mer-cury levels in seabirds and their fish prey at the Ebro Delta (NW Med-iterranean): the role of trawler discards as a source of contamination.Mar. Ecol. Prog. Ser. 232: 281–290.

Ashmole, N.P. 1971. Seabird ecology and the marine environment. InFarner, D.S. & King, J.R. (eds), Pages in Avian Biology, Vol. 1,pp. 224–271, Academic Press, New York.

Barquete, V., Bugoni, L. & Vooren, C.M. 2008. Diet of Neotropiccormorant (Phalacrocorax brasilianus) in an estuarine environment.Mar. Biol. 153: 431–443.

Barrett, R.T. 1991. Shags (Phalacrocorax aristotelis L.) as potentialsamplers of juvenile Saithe (Pollachius virens L.) stocks in NorthernNorway. Sarsia 76: 153–156.

Barrett, R.T. 2002. Atlantic Puffin Fratercula arctica and CommonGuillemot Uria aalge chick diet and growth as indicators of fish stocksin the Barents Sea. Mar. Ecol. Prog. Ser. 230: 275–287.

Barrett, R.T. & Furness, R.W. 1990. The prey and diving depths ofseabirds on Hørnoy, North Norway, after a decrease in the BarentsSea Capelin stocks. Ornis Scand. 21: 179–186.

Barrett, R.T., Strann, K.–B. & Vader, W. 1986. Notes on the eggsand chicks of North Norwegian Shags. Phalacrocorax aristotelis. Sea-bird 9: 3–10.

Barrett, R.T., Røv, N., Loen, J. & Montevecchi, W.A. 1990. Dietsof Shags Phalacrocorax aristotelis and Cormorants P. carbo in Nor-way and possible implications for gadoid stock recruitment. Mar.Ecol. Prog. Ser. 66: 205–218.

Barrett, R.T., Camphuysen, C.J., Anker–nilssen, T., Chardine,J.W., Furness, R.W., Garthe, S., Huppop, O. & Leopold,M.F. 2007. Diet studies of seabirds: a review and recommendations.ICES J. Mar. Sci. 26: 1675–1691.

Brichetti, P., De Franceschi, P. & Baccetti, N. 1992. Fauna d’Italia.Aves I, Gaviidae–Phasianidae: 99–120. Edizioni Calderini, Bologna.

Carss, D.N. 1993. Shags Phalacrocorax aristotelis at cage fish farms inArgyll, Western Scotland. Bird Study 40: 203–211.

Carss, D.N. & The Diet Assessment and Food Intake WorkingGroup 1997. Techniques for assessing Cormorant diet and food

intake: towards a consensus view. Supplemento Ricerche di Biologiadella Selvaggina 26: 197–230.

Cramp, S. & Simmons, K.L.S. 1977. The Birds of the WesternPalaearctic. Vol. 1: Ostrich to Ducks. Oxford University Press, Oxford.

Davoren, G.K. & Montevecchi, W.A. 2003. Signals from seabirdsindicate changing biology of capelin stocks. Mar. Ecol. Prog. Ser.258: 253–261.

Dirksen, S., Boudewijn, T.J., Noordhuis, R. & Marteijn, E.C.L.1995. Cormorants Phalacrocorax carbo sinensis in shallow eutrophicfreshwater lakes: prey choice and fish consumption in the non-breed-ing period and effects of large-scale fish removal. Ardea 83:167–184.

Duffy, D.C. & Jackson, S. 1986. Diet studies of seabirds: a review ofmethods. Colon. Waterbirds 9: 11–17.

Duffy, D.C. & Laurenson, I.J.R. 1983. Pellets of Cape Cormorants asindicators of diet. Condor 85: 305–307.

Eschbaum, R., Veber, T., Vetemaa, M. & Saat, T. 2003. Do cormor-ants and fishermen compete for fish resources in the Vainameri (easternBaltic) area? In Cowx, I.G. (ed.), Interactions Between Birds and Fish:Implications for Management: 72–83. Blackwell Science, Oxford.

Furness, R.W. & Camphuysen, C.J. 1997. Seabirds as monitors ofthe marine environment. ICES J. Mar. Sci. 54: 726–737.

Furness, R.W. & Tasker, M.L. 2000. Seabird–fishery interactions:quantifying the sensitivity of seabirds to reductions in sandeel abun-dance, and identification of key areas for sensitive seabirds in theNorth Sea. Mar. Ecol. Prog. Ser. 202: 253–264.

Gagliardi, A., Martinoli, A., Preatoni, D., Wauters, L.A. & Tosi,G. 2007. From mass to body elements to fish biomass: a directmethod to quantify food intake of fish eating birds. Hydrobiologia583: 213–222.

Gremillet, D., Argentin, G., Schulte, B. & Culik, B.M. 1998. Flex-ible foraging techniques in breeding Cormorants Phalacrocoraxcarbo and Shags Phalacrocorax aristotelis: benthic or pelagic feed-ing? Ibis 140: 113–119.

Guyot, I. 1988. Relationships between shag feeding areas and humanfishing activities in Corsica (Mediterranean Sea). In Tasker, M.L.(ed.), Seabird Food and Feeding Ecology: 22–23, Proceedings ofthe 3rd International Conference of the Seabird Group, Glasgow.

Guyot, I. 1993. Breeding distribution and number of Shag (Phalacrocoraxaristotelis desmarestii) in the Mediterranean. In Aguilar, J.S., Monabail-liu, X. & Paterson, A.M. (eds), Estatus y Conservacion de Aves Marinas:37–46, Actas del II Simposio MEDMARAVIS, SEO, Madrid.

Harkonen, T. 1986. Guide to the Otoliths of the Bony Fishes of theNortheast Atlantic, Danbiu, Aps Hellerup, Denmark.

Harris, M.P. & Wanless, S. 1991. The importance of the lesser san-deel Ammodytes marinus in the diet of the Shag. Phalacrocorax aris-totelis. Ornis Scand. 22: 375–383.

Harris, M.P. & Wanless, S. 1993. The diet of Shags Phalacrocoraxaristotelis during the chick-rearing period assessed by three methods.Bird Study 40: 135–139.

Hatch, S.A. & Sanger, G.A. 1992. Puffins as samplers of juvenile Pol-lock and other forage fish in the Gulf of Alaska. Mar. Ecol. Prog. Ser.80: 1–14.

Hislop, J.R.G. & Harris, M.P. 1985. Recent changes in the food ofyoung Puffins Fratercula arctica on the Isle of May in relation to fishstocks. Ibis 127: 234–239.

Johnstone, I.G., Harris, M.P., Wanless, S. & Graves, J.A. 1990.The usefulness of pellets for assessing the diet of adult shags. Phalacro-corax aristotelis. Bird Study 37: 5–11.

Jonsson, G. 1992. Icelandic Fishes, 2nd ed. Fjolvi, Reykjavik.Keller, T. 1993. Untersuchungen zur Nahrungsokologie von in Bayern

uberwinternden Kormoranen. Phalacrocorax carbo sinensis. Orn.Verh. 25: 811–828.

Q 2011 British Trust for Ornithology, Bird Study, iFirst, 1–12

Diet of Mediterranean Shags 11

Dow

nloa

ded

by [

Mau

ro C

osol

o] a

t 23:

27 0

6 O

ctob

er 2

011

Lambertini, M. &Leonzio, C. 1986. Pollutant levels and their effects onMediterranean seabirds, In: MEDMARAVIS & Monabailliu, X. (eds).Mediterranean Marine Avifaun, pp. 359–378. Springer-Verlag,Berlin–Heidelberg.

Lilliendahl, K. & Solmundsson, J. 2006. Feeding ecology of sympa-tric European Shags Phalacrocorax aristotelis and Great CormorantsP. carbo in Iceland. Mar. Biol. 149: 979–990.

Louisy, P. 2005. Guida all’identificazione dei Pesci Marini d’Europa edel Mediterraneo, Il Castello, Milano, Italy.

Mannini, P., Massa, F. & Milone, N. 2005. Adriatic Sea Fisheries:outline of some main facts. In Cataudella, S., Massa, F. & Crosetti,D. (eds), Interactions Between Aquaculture and Capture Fisheries: AMethodological Perspective, General Fisheries Commission for theMediterranean, Rome.

Miller, A. & Sydeman, W.J. 2004. Rockfish response to low frequencyocean climate change as revealed by the diet of a marine bird overmultiple time scales. Mar. Ecol. Prog. Ser. 281: 207–216.

Mills, K.L., Laidig, T., Ralston, S. & Sydeman, W. 2007. Diets oftop predators indicate pelagic juvenile rockfish (Sebastes spp.) abun-dance in the California Current System. Fish. Oceanogr. 16:273–283.

Montevecchi, W.A. 1993. Birds as indicators of change in marine preystocks. In Furness, R.W. & Greenwood, J.J.J. (eds), Birds as Monitorsof Environmental Change: 219–266. Chapman and Hall, London.

Montevecchi, W.A. & Myers, R.A. 1996. Dietary changes of sea-birds indicate shifts in pelagic food webs. Sarsia 80: 313–322.

Nelson, B.J. 2005. Pelicans, Cormorants, and their Relatives. The Pele-caniformes. Oxford University Press, Oxford.

Orel, G. & Zamboni, R. 2004. Proposte per un piano pluriennale digestione della fascia costiera del Golfo di Trieste. II Edizione rivedutaed ampliata. ARIES—Progetto Pesca, SFOP 2000–2003.

Oro,D.&Ruiz,X.1997. Exploitation of trawler discards by breeding sea-birds in the north-western Mediterranean: differences between the EbroDelta and the Balearic Islands areas. ICES J. Mar. Sci. 54: 695–707.

Patzner, R.A. 2007. Mediterranean gobies. Availabel from: www.users.sbg.ac.at/~patzner/Gobiidae.htm [accessed 31 March 2011].

Prestamburgo, M., Cosmina, M., Gallenti, G., Mauro, L. &Girardini, C. 2005. Progetto ADRI.FISH. Realizzazione della retedi monitoraggio dati ‘L’economia della pesca entro le tre miglia nel-l’area Adri.Fish’. PIC Interreg IIIB Cadses. Dipartimento di Economiae Tecnica aziendale, Universita degli Studi di Trieste, Trieste.

Privileggi, N. 2003. Great Cormorants Phalacrocorax carbo sinensiswintering in Friuli Venezia Giulia, Northern Adriatic: specific andquantitative diet composition. Vogelwelt 124: 237–243.

Riedl, R. 1991. Fauna e Flora del Mediterraneo. Franco Muzzio Editore,Padova, Italy.

Rindorf, A., Wanless, S. & Harris, M.P. 2000. Effects of changes insandeel availability on the reproductive output of seabirds. Mar. Ecol.Prog. Ser. 202: 241–252.

Roth, J.E., Mills, K.L. & Sydeman, W.J. 2007. Chinook salmon(Oncorhynchus tshawytscha) – seabird covariation off central Califor-nia and possible forecasting applications. Can. J. Fish. Aquat. Sci.64: 1080–1090.

Skrivanic, A. & Zavodnik, D. 1973. Migration of the sardine Sardinapilchardus in relation to hydrographical conditions of the AdriaticSea. Neth. J. Sea Res. 7: 7–18.

Sponza, S., Cimador, B., Cosolo, M. & Ferrero, E.A. 2010. Divingcosts and benefits during post-breeding movements of the Mediterra-nean Shag in the North Adriatic Sea. Mar. Biol. 157: 1203–1213.

Steven, J. 1933. The food consumed by shags and cormorants aroundshores of Cornwall (England). J. Mar. Biol. Ass. UK 19: 277–292.

Thayer, J.A. & Sydeman, W.J. 2007. Spatio-temporal variability inprey harvest and reproductive ecology of a piscivorous predator Cer-orhinca monocerata in an upwelling system. Mar. Ecol. Prog. Ser.329: 253–265.

Utmar, P. 1999. Marangone dal ciuffo Phalacrocorax aristotelis. In Par-odi, R. (ed.), Gli uccelli della provincia di Gorizia, (Vol. 42: pp.44–45. Edizioni Museo Friulano di Storia Naturale, Udine.

Velando, A. 1997. Ecologia y comportamiento del cormoran monudoPhalacrocorax aristotelis en las Islas Cies y Ons. PhD thesis. Universityof Vigo, Spain.

Velando, A. & Freire, J. 1999. Intercolony and seasonal differences inthe breeding diet of European Shags on the Galician coast (NWSpain). Mar. Ecol. Prog. Ser. 188: 225–236.

Velando, A. & Freire, J. 2002. Population modelling of EuropeanShags (Phalacrocorax aristotelis) at their southern limit: conservationimplications. Biol. Conserv. 107: 59–69.

Velando, A., Alvarez, D., Mourino, J., Arcos, F. & Barros, A.2005. Population trends and reproductive success of the EuropeanShag Phalacrocorax aristotelis on the Iberian Peninsula followingthe Prestige oil spill. J. Ornithol. 146: 116–120.

Veldkamp, R. 1995. The use of chewing pads for estimating the con-sumption of cyprinids by Cormorants Phalacrocorax carbo. Ardea83: 135–138.

Volponi, S. 1994. Ecologia del Cormorano Phalacrocorax carbo sinen-sis nel Delta del fiume Po. PhD Thesis, University of Ferrara, Italy.

Wanless, S., Burger, A.E. & Harris, M.P. 1991a. Diving depths ofshags Phalacrocorax aristotelis breeding on Isle of May. Ibis 133:37–42.

Wanless, S., Harris, M.P. & Morris, J.A. 1991b. Foraging rangeand feeding locations of Shags (Phalacrocorax aristotelis) duringchick rearing. Ibis 133: 30–36.

Wanless, S., Corfield, T., Harris, M.P., Buckland, S.T. & Morris,J.A. 1993a. Diving behaviour of the Shag Phalacrocorax aristotelis inrelation to water depth and prey size. J. Zool. 231: 11–25.

Wanless, S., Harris, M.P. & Russell, S. 1993b. Factors influencingfood-load sizes brought in by Shags Phalacrocorax aristotelis duringchick rearing. Ibis 135: 19–24.

Wanless, S., Harris, M.P., Burger, A.E. & Buckland, S.T. 1997a.Use of time-at-depth recorders for estimating depth and diving per-formance of European Shags. J. Field Ornithol. 68: 547–561.

Wanless, S., Bacon, P.J., Harris, M.P., Webb, A.D., Green-street, S.P.R. & Webb, A. 1997b. Modelling environmental andenergetic effects on feeding performance and distribution of Shag(Phalacrocorax aristotelis): integrating telemetry, geographical infor-mation system, and modelling techniques. ICES J. Mar. Sci. 54:524–544.

Wanless, S., Gremillet, D. & Harris, M.P. 1998. Foraging activityand performance of Shag Phalacrocorax aristotelis in relation toenvironmental characteristics. J. Avian Biol. 29: 49–54.

Wanless, S., Harris, M.P., Redman, P. & Speakman, J.R. 2005.Low energy values of fish as a probable cause of a major seabirdbreeding failure in the North Sea. Mar. Ecol. Prog. Ser. 294: 1–8.

Watanuki, Y., Daunt, F., Takahashi, A., Newell, M., Wan-less, S., Satom, K. & Miyazaki, N. 2008. Microhabitat useand prey capture of a bottom-feeding top predator, the EuropeanShag, shown by camera loggers. Mar. Ecol. Prog. Ser. 356:283–293.

(MS received 18 April 2011; revised MS accepted 4 July 2011)

Q 2011 British Trust for Ornithology, Bird Study, iFirst, 1–12

12 M. Cosolo et al.

Dow

nloa

ded

by [

Mau

ro C

osol

o] a

t 23:

27 0

6 O

ctob

er 2

011